Hybridization alters the shape of the genotypic fitness landscape, increasing access to novel fitness peaks during adaptive radiation.

Estimating the complex relationship between fitness and genotype or phenotype (i.e. the adaptive landscape) is one of the central goals of evolutionary biology. However, adaptive walks connecting genotypes to organismal fitness, speciation, and novel ecological niches are still poorly understood and processes for surmounting fitness valleys remain controversial. One outstanding system for addressing these connections is a recent adaptive radiation of ecologically and morphologically novel pupfishes (a generalist, molluscivore, and scale-eater) endemic to San Salvador Island, Bahamas. We leveraged whole-genome sequencing of 139 hybrids from two independent field fitness experiments to identify the genomic basis of fitness, estimate genotypic fitness networks, and measure the accessibility of adaptive walks on the fitness landscape. We identified 132 single nucleotide polymorphisms (SNPs) that were significantly associated with fitness in field enclosures. Six out of the 13 regions most strongly associated with fitness contained differentially expressed genes and fixed SNPs between trophic specialists; one gene (mettl21e) was also misexpressed in lab-reared hybrids, suggesting a potential intrinsic genetic incompatibility. We then constructed genotypic fitness networks from adaptive alleles and show that scale-eating specialists are the most isolated of the three species on these networks. Intriguingly, introgressed and de novo variants reduced fitness landscape ruggedness as compared to standing variation, increasing the accessibility of genotypic fitness paths from generalist to specialists. Our results suggest that adaptive introgression and de novo mutations alter the shape of the fitness landscape, providing key connections in adaptive walks circumventing fitness valleys and triggering the evolution of novelty during adaptive radiation.

One of the main drivers of evolution is natural selection, which is when organisms better adapted to their environment are more likely to survive and reproduce. A common metaphor to explain this process is a landscape covered in peaks and valleys: the peaks represent genetic combinations or traits with high evolutionary fitness, while the valleys represent those with low fitness. As a population evolves and its environment changes, it moves among these peaks taking small steps across the landscape. However, there is a limit to how far an organism can travel in one leap. So, what happens when they need to cross a valley of low fitness to get to the next peak? To address this question, Patton et al. studied three young species of pupfish that recently evolved from a common ancestor and co-habit the same environment in the Caribbean. Patton et al. sequenced whole genomes of each new species and used this to build a genotypic fitness landscape, a network linking neighboring genotypes which each have a unique fitness value that was measured during field experiments. This revealed that most of the paths connecting the different species passed through valleys of low fitness. But there were rare, narrow ridges connecting each species. Next, Patton et al. found that new mutations as well as genetic variations that arose from mating with pupfish on other Caribbean islands altered genetic interactions and changed the shape of the fitness landscape. Ultimately, this significantly increased the accessibility of fitness peaks by both adding more ridges and decreasing the lengths of paths, expanding the realm of possible evolutionary outcomes. Understanding how fitness landscapes change during evolution could help to explain where new species come from. Other researchers could apply the same approach to estimate the genotypic fitness landscapes of other species, from bacteria to vertebrates. These networks could be used to visualize the complex fitness landscape that connects all lifeforms on Earth.

Surprising spatiotemporal stability of a multi-peak fitness landscape revealed by independent field experiments measuring hybrid fitness.

The effect of the environment on fitness in natural populations is a fundamental question in evolutionary biology. However, experimental manipulations of both environment and phenotype at the same time are rare. Thus, the relative importance of the competitive environment versus intrinsic organismal performance in shaping the location, height, and fluidity of fitness peaks and valleys remains largely unknown. Here, we experimentally tested the effect of competitor frequency on the complex fitness landscape driving adaptive radiation of a generalist and two trophic specialist pupfishes, a scale-eater and molluscivore, endemic to hypersaline lakes on San Salvador Island (SSI), Bahamas. We manipulated phenotypes, by generating 3407 F4/F5 lab-reared hybrids, and competitive environment, by altering the frequency of rare transgressive hybrids between field enclosures in two independent lake populations. We then tracked hybrid survival and growth rates across these four field enclosures for 3-11 months. In contrast to competitive speciation theory, we found no evidence that the frequency of hybrid phenotypes affected their survival. Instead, we observed a strikingly similar fitness landscape to a previous independent field experiment, each supporting multiple fitness peaks for generalist and molluscivore phenotypes and a large fitness valley isolating the divergent scale-eater phenotype. These features of the fitness landscape were stable across manipulated competitive environments, multivariate trait axes, and spatiotemporal heterogeneity. We suggest that absolute performance constraints and divergent gene regulatory networks shape macroevolutionary (interspecific) fitness landscapes in addition to microevolutionary (intraspecific) competitive dynamics. This interplay between organism and environment underlies static and dynamic features of the adaptive landscape.